Trait anxiety and the neural efficiency of manipulation in working memory.

Basten U, Stelzel C, Fiebach CJ - Cogn Affect Behav Neurosci (2012)

Bottom Line:
Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex.We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency.Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.

ABSTRACTThe present study investigates the effects of trait anxiety on the neural efficiency of working memory component functions (manipulation vs. maintenance) in the absence of threat-related stimuli. For the manipulation of affectively neutral verbal information held in working memory, high- and low-anxious individuals (N = 46) did not differ in their behavioral performance, yet trait anxiety was positively related to the neural effort expended on task processing, as measured by BOLD signal changes in fMRI. Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex. Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex. We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency. With respect to the functions of working memory, we conclude that anxiety specifically impairs the processing efficiency of (control-demanding) manipulation processes (as opposed to mere maintenance). Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.

Fig4: Functional connectivity of the right DLPFC in the working memory manipulation task. The x- and z-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package, and the statistical parametric maps in panels B and C are shown at a voxel-level threshold of p < .005. (a) Seed region in right DLPFC. (b) Functional connectivity of the right DLPFC across participants, clusters show enhanced coupling with right DLPFC for manipulation > maintenance. (c) Positive association of anxiety and functional connectivity, controlling for (nonsignificant) variation in performance. The clusters show stronger PPI with DLPFC in high- as compared to low-anxious participants. (d) Individual strength of PPI with DLPFC, plotted against anxiety.performance—that is, the residual of trait anxiety from regression on behavioral performance. The PPI estimates derive from the contrast value of the interaction regressor in the PPI model. The scale of the ordinate given in the plot to the left is valid for both plots. DACC, dorsal anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; IPS, intraparietal sulcus; Precun, precuneus; SFS, superior frontal sulcus; VLPFC, ventrolateral prefrontal cortex; L, left; R, right. *Note that seed connectivity with left VLPFC was significantly modulated by anxiety only in the regression model including intelligence

Mentions:
Across participants—not taking into account differences in trait anxiety—a subset of the areas identified as activated during working memory manipulation (see above and in Fig. 2) showed increased functional connectivity with the right DLPFC seed region (Fig. 4a) during the task delay period. For the experimental condition of interest (i.e., manipulation), as contrasted to the control condition (maintenance), activity in the right DLPFC seed region showed enhanced coupling with activity in the left DLPFC (including medial frontal gyrus and the adjacent inferior and superior frontal gyrus), the dorsal ACC, the posterior part of the SFS bilaterally, left IPS, medial parts of the precuneus bilaterally, and superior parts of the right cerebellum (p < .05, corrected; see Table 3 and Fig. 4b). Functional connectivity across participants for left IFS and rACC is reported in the supplementary materials (Table S4).Fig. 4

Fig4: Functional connectivity of the right DLPFC in the working memory manipulation task. The x- and z-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package, and the statistical parametric maps in panels B and C are shown at a voxel-level threshold of p < .005. (a) Seed region in right DLPFC. (b) Functional connectivity of the right DLPFC across participants, clusters show enhanced coupling with right DLPFC for manipulation > maintenance. (c) Positive association of anxiety and functional connectivity, controlling for (nonsignificant) variation in performance. The clusters show stronger PPI with DLPFC in high- as compared to low-anxious participants. (d) Individual strength of PPI with DLPFC, plotted against anxiety.performance—that is, the residual of trait anxiety from regression on behavioral performance. The PPI estimates derive from the contrast value of the interaction regressor in the PPI model. The scale of the ordinate given in the plot to the left is valid for both plots. DACC, dorsal anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; IPS, intraparietal sulcus; Precun, precuneus; SFS, superior frontal sulcus; VLPFC, ventrolateral prefrontal cortex; L, left; R, right. *Note that seed connectivity with left VLPFC was significantly modulated by anxiety only in the regression model including intelligence

Mentions:
Across participants—not taking into account differences in trait anxiety—a subset of the areas identified as activated during working memory manipulation (see above and in Fig. 2) showed increased functional connectivity with the right DLPFC seed region (Fig. 4a) during the task delay period. For the experimental condition of interest (i.e., manipulation), as contrasted to the control condition (maintenance), activity in the right DLPFC seed region showed enhanced coupling with activity in the left DLPFC (including medial frontal gyrus and the adjacent inferior and superior frontal gyrus), the dorsal ACC, the posterior part of the SFS bilaterally, left IPS, medial parts of the precuneus bilaterally, and superior parts of the right cerebellum (p < .05, corrected; see Table 3 and Fig. 4b). Functional connectivity across participants for left IFS and rACC is reported in the supplementary materials (Table S4).Fig. 4

Bottom Line:
Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex.We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency.Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.

ABSTRACTThe present study investigates the effects of trait anxiety on the neural efficiency of working memory component functions (manipulation vs. maintenance) in the absence of threat-related stimuli. For the manipulation of affectively neutral verbal information held in working memory, high- and low-anxious individuals (N = 46) did not differ in their behavioral performance, yet trait anxiety was positively related to the neural effort expended on task processing, as measured by BOLD signal changes in fMRI. Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex. Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex. We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency. With respect to the functions of working memory, we conclude that anxiety specifically impairs the processing efficiency of (control-demanding) manipulation processes (as opposed to mere maintenance). Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.